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CELL BIOLOGY & MOLECULAR GENETICS

Identification of a QTL Associated with Tolerance of Soybean to Soil Waterlogging

^a USDA-ARS, Soil Drainage Research, Columbus, OH 43210
^b Dep. Horticulture and Crop Science, The Ohio State Univ., Columbus, OH 43210
^c Dep. of Plant Pathology, Ohio Agricultural Research and Development Center, Wooster, OH 44691
^d Dep. of Biology, Univ. of Utah, Salt Lake City, UT 84112

* Corresponding author (vantoai.1{at}osu.edu)

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIAL AND METHODS RESULTS DISCUSSION REFERENCES

 
Soil waterlogging is a major environmental stress that suppresses soybean [Glycine max (L.) Merr.] growth and yield. Our objective was to identify quantitative trait loci (QTL) associated with the tolerance of soybean to soil waterlogging. We subjected 208 lines of two recombinant inbred (RI) populations, ‘Archer’ x ‘Minsoy’ and ‘Archer’ x ‘Noir I’, to 2 wk of waterlogging when the plants were at the early flowering stage. The control plants were not flooded. The experiment was conducted in three environments: Columbus, OH, in 1997 and 1998 and Wooster, OH, in 1998. We identified a single QTL, linked to marker Sat_064, from the Archer parent which was associated with improved plant growth (from 11–18%) and grain yields (from 47–180%) in waterlogged environments. This highly significant QTL (P = 0.02–0.000001) was identified in both RI populations and at both Columbus 1997 and 1998 environments, but not at the Wooster 1998 environment. The differences in soil type and flooding treatment (stagnant versus moving water) could have contributed to the lack of QTL identification at the Wooster 1998 environment. The Sat_064 QTL was uniquely associated with waterlogging tolerance and was not associated with maturity, normal plant height or grain yields. The Sat_064 marker maps close to the Rps4 gene for Phytophthora (Phytophthora sojae M.J. Kaufmann & J.W. Gerdemann) resistance; however, since Archer does not contain the Rps4 resistance allele, it is probably not a disease tolerance QTL. Near isogenic lines with and without the Sat_064 marker have been developed and are being field tested under waterlogging conditions to confirm the association of the QTL with the tolerance of soybean to waterlogging stress.

Abbreviations: ANOVA, analysis of variance • CO97, 1997 Columbus environment • CO98, 1998 Columbus environment • QTL, quantitative trait loci • RIL, recombinant inbred lines • WO98, 1998 Wooster environment

	INTRODUCTION

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PERIODIC FLOODING during the growing season adversely affects soybean growth and grain production in many areas of the USA and the rest of the world. (Stanley et al., 1980; Oosterhuis et al., 1990). Soil can become flooded when it is poorly drained or when rainfall or irrigation is excessive. Other terms, such as soil saturation, waterlogging, anoxia, and hypoxia are also commonly used to describe flooding conditions. Flooding causes premature senescence which results in leaf chlorosis, necrosis, defoliation, reduced nitrogen fixation, and cessation of growth and reduced yield (Daugherty and Musgrave, 1994; Linkemer et al., 1998; VanToai et al., 1994; Bacanamwo and Purcell, 1999). In general, there are two types of flooding: waterlogging, where the root and a portion of the shoot are flooded, and complete submergence, where the entire plants are under water. Soil waterlogging for as little as 2 d reduced soybean yield by 18% at the late vegetative growth stage and 26% at the early reproductive stage (Scott et al., 1989).

In the last two decades, a great deal of information has accumulated from research on the molecular, biochemical, physiological, anatomical, and morphological responses of plants to flooding and anoxia (Kennedy et al., 1992; Perata and Alpi, 1993; Ricard et al., 1994; Crawford and Brandle, 1996; Vartapetian and Jackson, 1997). While the lack of oxygen has been proposed as the main problem associated with flooding (Ponnamperuma, 1972; Trought and Drew, 1980), growth reduction and yield loss during and after flooding could also arise from root rot diseases (Schmitthenner, 1985), nitrogen deficiency (Fausey et al., 1985), or nutrient imbalance (Hendry and Brocklebank, 1985; Thomson et al., 1989; Barrick and Noble, 1993). Recently, the accumulation of root zone CO₂ has been implicated as a cause of flooding injuries in soybean (Boru et al., 1997).

While the ability to produce high seed yield in flooded fields is the ultimate criterion of flooding tolerance, other traits, including leaf color, plant height, root, and shoot biomass, have been used frequently as determinants of flooding tolerance (Daugherty and Musgrave, 1994). However, attempts to apply this knowledge to the development of flood-tolerant crop cultivars have not yet been successful. Having elite high-yield soybean cultivars that are flood tolerant will reduce year-to-year yield variation and greatly benefit farmers. Genetic variability for flooding tolerance exists in soybean (VanToai et al., 1994). Tolerance to flooding in wheat (Triticum aestivum L.) and rice (Oryza sativa L.) is a quantitative trait controlled by a small number of genes (Boru et al., 2001; Setter et al., 1997). Xu and Mackill (1996) identified a random amplified polymorphic DNA (RAPD) marker that accounted for 50% of the variation in submergence tolerance of rice. The result was confirmed by an amplified fragment length polymorphism (AFLP) marker which mapped to the same area (Nandi et al., 1997).

During the last few years, molecular marker aided-selection has been used successfully for the breeding of crops with improved quantitative traits (Stuber, 1994). The objective of this research was to identify the QTLs associated with waterlogging tolerance of soybean. Molecular markers linked to these can be identified and be used to facilitate the development of flood-tolerant elite soybean cultivars by molecular plant breeding.

	MATERIAL AND METHODS

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Genetic Materials
One hundred twenty-two recombinant inbred lines (RIL) of the Archer x Minsoy and 86 RIL of the Archer x Noir I populations were used in this study. Archer is more tolerant to waterlogging than Minsoy and Noir I. The lines were selected from a larger set of RIL with maturity (group II or later) as the sole selection criterion. The populations were developed by Dr. Levi Mansur and had been inbred for nine generations. Each of the parents and RIL were characterized for the parental alleles with over 600 genetic markers including morphological traits, restriction fragment length polymorphism (RFLP), AFLP, and simple sequence repeats (SSR) (Cregan et al., 1999; Orf et al., 1999).

Field Experiments
Location and Soil Type
The study was conducted at the Ohio State University Waterman farm at Columbus, OH, in 1997 (CO97) and 1998 (CO98) and at the Ohio Agricultural Research and Development Center Snyder farm at Wooster, OH, in 1998 (WO98). The Waterman farm is located at latitude 39°59'N, longitude 83°01'W, and elevation 240 m. The soil type is a Kokomo silty clay loam (fine, mixed, mesic Typic Argiaquolls) with moderately slow permeability. The Snyder farm is located at latitude 40°47'N, longitude 81°55'W and elevation 306 m. Its soil type is a poorly drained Canfield silt loam (fine-loamy, mixed, mesic, Aquic Fragiudalfs).

Experimental Design and Statistical Analysis
The overall design of the experiment was a split-plot with the flooding treatments (i.e., waterlogged and control) as the whole-plot factor and genotypes assigned to sub-plots. In each of the three environments there was a single waterlogged field and an adjacent control field. Thus, environments served as replicates for the flooding treatments. At both locations, the waterlogged treatment was applied to a field that was leveled prior to the beginning of the study in 1997. In this field, the topsoil was removed and the sub-soil leveled to within ±3 cm. The topsoil was then reapplied and leveled. At Columbus, the leveled field was large enough to allow crop rotation. Half of the leveled field was used in the 1997 flooded treatment, while the other half was used in the 1998 flooded treatment.

Within each flooding treatment, genotypes were arranged in an augmented randomized complete block design. At Columbus, there were 15 blocks in 1997 and 17 in 1998. Each block consisted of 20 plots, of which five were assigned the parents and check cultivars (Archer, Minsoy, Noir, ‘IA2007’, and ‘Conrad’), and the remaining 15 were assigned individual RI lines. Of the two checks, IA2007 was a breeding line with flooding tolerant potential, while Conrad is an Ohio standard public cultivar. A few extra genotypes not related to this experiment were added in 1998, accounting for the 16th and 17th blocks. At Wooster, there were 18 blocks, each with 18 plots. In each block, there was one plot of each parent or check (Archer, Minsoy, Noir, and IA2007). The remaining 14 plots were allocated to individual RI lines. Use of an augmented design for genotypes allowed us to estimate an experimental error, based on the replicated checks and parents, for each combination of environment and flooding treatment.

Planting dates were 7 May 1997 and 2 June 1998 at Columbus and 15 May 1998 at Wooster. Plots consisted of a single row, 1 m long, with 40 plants per row. Row spacing was 75 cm. No fertilizer was used, based on soil tests. Herbicides were applied as needed.

Flooding Treatment
The plants were subjected to soil waterlogging for 2 wk when 50% of the RI lines were at the early flowering (R1) growth stage (Fehr and Caviness, 1977). At the Columbus site, soil waterlogging was imposed by overhead irrigation and subirrigation (Fausey, 1994) to raise the water table to 5 to 10 cm above the soil surface. At the Wooster site, soil waterlogging was imposed by overhead irrigation alone. The control plots were irrigated as needed to avoid drought stress.

Soil Analysis
At each sampling time (before, during and after flooding), six soil samples were randomly collected in each plot to approximately 0.18-m depth with a 2.5-cm diam soil probe. The samples from each plot were combined, air dried, ground and analyzed for pH (1:1 water) (McLean, 1982). Soil chemical analyses to determine P, K, Ca, and Mg concentrations were conducted as described by Warncke and Brown (1998) at the Service Testing and Research Laboratory, Ohio Agricultural Development and Research Center, Wooster, OH.

Determination of Flooding Tolerance
Flooding responses were determined by plant growth and seed yield. To determine growth, plant height was taken just before flooding at about 8 wk after planting (early plant height) and 1 d after the flooding stress was removed (late plant height). At Columbus, maturity of each plot was recorded as the number of days after 31 July when 95% of the pods had reached their mature color. Maturity was not determined at the Wooster site. At the end of the season, the seeds were harvested by hand and seed yield determined.

Data Analysis and Mapping of QTL
Each of the environment-flooding treatment combinations was analyzed first as an augmented design to obtain genotype means, adjusted for blocks. We did not attempt to analyze the waterlogged and control portions of the full experiment in a single analysis. Rather, phenotypic means for waterlogged and control traits were mapped separately, with the idea of identifying markers that indicated QTL for traits under waterlogged conditions but that had no effect in the control condition.

Combined analysis of the three environments was complicated by heterogeneity of error across environments, which was apparent for all traits except maturity. To account for this, we used a mixed model analysis with location as a random factor and genotype as a fixed factor. For the diagonal of the variance-covariance matrix we used the error variance for each location, divided by the number of replications for the genotype in question (i.e., the number of blocks for a check or parent, 1 for a RI). Generalized least squares means for each RI, across locations, were used for mapping and correlation analysis. Correlation analysis was performed by SAS Software Package (SAS Institute Inc., Cary, NC) to quantify the degree of positive or negative linear relationship between the average trait means under flooded and nonflooded conditions.

Mapping was carried out for each location separately, with block-adjusted means. QTL for tolerance to soil waterlogging were identified and analyzed for interactions by the Epistat computer program (Chase et al., 1997). This computer software uses maximum likelihood methods and permutation tests for both the identification and evaluation of significance of interactions between pairs of QTLs (Chase et al., 1997). The simple interval mapping feature of the computer package PLABQTL (Utz and Melchinger, 1996), was also used for detecting QTL. This program uses a multiple regression approach to interval mapping with marker order and distances determined by MapMaker (Lander et al., 1987; Lincoln et al., 1993).

The empirical LOD thresholds for QTL detection was established using permutation tests (Churchill and Doerge, 1994). The Minsoy x Archer cross consists of 102 plants genotyped with 370 markers. The single marker threshold estimated to give a false positive rate of 0.05 was LOD 3.18; P-value 0.00066. The threshold for interactions was estimated at LOD 4.4; P-value 0.00004. The Noir x Archer cross consists of 75 plants genotyped with 347 markers. The single marker threshold estimated to give a false positive rate of 0.5 was LOD 3.17; P-value 0.00066. The threshold for interactions was estimated at LOD 4.4; P-value 0.00004. No significant interaction was detected.

	RESULTS

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Weather Conditions
At the Columbus site, the average temperature for the 1997 growing season from May 1 to September 30 was 17.6°C and was 1.3°C lower than the 20-yr historical average temperature (18.9°C). The 68.6 cm of total precipitation for the 5-mo growing season was 7.9 cm higher than the 20-yr historical precipitation. In 1998, the average temperature for the 5-mo growing season was 20°C which was 1°C warmer than the historical average, while the total precipitation of 35.8 cm was much lower than the historical precipitation of 60.7 cm. In 1998, the average temperature of the Wooster site was 18.5°C and was 1.1°C warmer than the historical average of 17.3°C. 1998 was also a dry year for the Wooster site with a total precipitation of 48.0 cm as compared with the historical precipitation of 56.1 cm.

Effects of Waterlogging
Responses of the parents and IA2007 to the waterlogging treatment are reported in Table 1. The average maturity of Minsoy and Noir I in the control treatment was similar, but Archer matured 10 to 15 d later (P = 0.05). Waterlogging did not alter the maturity of Archer and Minsoy but hastened the maturity of Noir I by 6 d (P = 0.05). Similarly, waterlogging also hastened the maturity of IA2007 by 8 d (P = 0.05).

Waterlogging for 2 wk at the flowering stage significantly reduced the late plant height of Minsoy by 16%, of Noir I by 23% and of Archer and IA2007 by 27 and 28%, respectively, as compared with the nonflooded plant height.

The effects of waterlogging were much more severe on grain yield than on plant height. Waterlogging for 2 wk reduced grain yield of Archer the least (69%), followed by Minsoy (75%), while the grain yield of Noir I was reduced by 84% relative to control yield. The grain yield of IA2007 was reduced by 77% after 2 wk of flooding.

The correlation between control grain yield and flooded grain yield was not significant across the two populations and three environments (Table 2). The correlation between late plant height and grain yield was significant (P = 0.05) but smaller in the control (R = 0.32) than in the waterlogged treatment (R = 0.53). The correlation between maturity and grain yield was significant in the control treatment (R = 0.23), but not significant in the waterlogged treatment (R = 0.16).

The Archer Sat_064 allele was not associated with any other traits that were determined in the waterlogging treatment including flooded maturity and flooded early plant height. The allele was also not associated with grain yield, maturity, early plant height, or late plant height of the control treatment.

	DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIAL AND METHODS RESULTS DISCUSSION REFERENCES

 
A single QTL marked with Sat_064 was associated with taller plant and greater grain yield of waterlogged plants of both RI populations in both years (1997 and 1998) at the Columbus location. The fact that the same QTL affected both growth and grain yield under waterlogged conditions indicated that plants that grew better during the 2-wk waterlogging stress (i.e., taller) also produced more grain at the end of the growing season. Flooded plant height has been used as indicator of flooding tolerance (Daugherty and Musgrave, 1994). This study confirms the relatedness (R = 0.53) between flooded plant height and flooded grain yield (Table 2), the ultimate criterion of flooding tolerance in production agriculture. However, while Sat_064 was a strong marker which explained from 22 to 33% of the variation in grain yield of the two populations, it only explained 8 to 9% of the variation in flooded plant height (Table 4).

The Sat_064 marker was specific for flooding tolerance and was not associated with growth and grain yield under nonflooded, control conditions. The Sat_064 marker is mapped to the linkage group G of the USDA soybean linkage map (Cregan et al., 1999). The Rps4 gene for Phytophthora resistance is also mapped to the same position linkage group. While Archer contains the Rps1k and Rps6 genes, it does not contain the Rps4 gene. In addition, no visible disease symptoms were detected in the CO97 and CO98 environment. Nevertheless, the possibility that the Sat_064 QTL is associated with the tolerance of a flooding related disease cannot be ruled out. Indeed, some preliminary linkage data suggest that Rps6 is located in the vicinity of the Sat_064 allele (Demirbas et al., 2001)

The fact that the Sat_064 QTL was not identified at the Wooster site was perplexing. The flooding treatment at the Columbus site was imposed by subirrigation to raise the water table from below the ground. During the flooding treatment, the water was stagnant. At the Wooster site, flooding was imposed by continuous overhead irrigation. The flooded plots at that site were on high ground and water was constantly moving through the soil profile during the flooding treatment. According to Heatherly and Pringle (1991), stagnant flooding was more injurious to soybean growth and yield than flooding with moving water. It has been documented that the low-lying areas of many fields are usually highly compacted due to the loss of soil structures resulting from farm machinery traffic on wet soil (Fausey and Lal, 1990). Natural flooding that occurs in these areas is probably more similar to the flooding stress at the Columbus site than at the Wooster site.

While the Sat_064 effect was detected in both populations and in both CO97 and CO98 environments, the effects of the QTL on flooded grain yield and plant height were much larger in the CO97 environment than in CO98 environment. After the field leveling in 1997, soil of the flooded plots in Columbus was highly compacted as indicated by the depressed growth and yield. The flooded plots were deep plowed in the spring of 1998 before planting which significantly improved grain yield. It is possible that the Sat_064 QTL was associated with depressed growth and yield due to compacted and flooded soil.

Flooding did not change the soil P, K, Ca, and Mg concentrations at either Columbus or Wooster. However, the soil at the Columbus site was one pH unit higher and contained three to four times more P, K, Ca, and Mg than the soil in Wooster (Table 5). Since the overall flooded yield at the WO98 environment was not different from that at the CO98 environment, soil fertility was probably not a determining factor affecting the identification of the flood-tolerance QTL at that site.

	ACKNOWLEDGMENTS

 
We thank Dr. Anne Dorrance and Ms. Sue Ann McClure of Department of Plant Pathology for the help with field work. Thanks are also due to Dr. James Orf of University of Minnesota for supplying the seeds and to Dr. Levi Mansur of Catholic University, Chile, for the development of the RI populations.

	NOTES

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Funded in part by grants from The United Soybean Board, The Ohio Soybean Council and The Ohio Agricultural Research and Development Center. Use of trade names is for the benefit of readers and does not imply endorsement of the product by the U.S. Dep. of Agric. Joint contribution of the USDA-ARS and The Ohio State Univ. Salaries and research support provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State Univ. Manuscript number HCS00-6.

Received for publication August 1, 2000.

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